Neuroanatomy of the late Cretaceous Thescelosaurus neglectus (Neornithischia: Thescelosauridae) reveals novel ecological specialisations within Dinosauria

Ornithischian dinosaurs exhibited a diversity of ecologies, locomotory modes, and social structures, making them an ideal clade in which to study the evolution of neuroanatomy and behaviour. Here, we present a 3D digital reconstruction of the endocranial spaces of the latest Cretaceous neornithischian Thescelosaurus neglectus, in order to interpret the neuroanatomy and paleobiology of one of the last surviving non-avian dinosaurs. Results demonstrate that the brain of Thescelosaurus was relatively small compared to most other neornithischians, instead suggesting cognitive capabilities within the range of extant reptiles. Other traits include a narrow hearing range, with limited ability to distinguish high frequencies, paired with unusually well-developed olfactory lobes and anterior semicircular canals, indicating acute olfaction and vestibular sensitivity. This character combination, in conjunction with features of the postcranial anatomy, is consistent with specializations for burrowing behaviours in the clade, as evidenced by trace and skeletal fossil evidence in earlier-diverging thescelosaurids, although whether they reflect ecological adaptations or phylogenetic inheritance in T. neglectus itself is unclear. Nonetheless, our results provide the first evidence of neurological specializations to burrowing identified within Ornithischia, and non-avian dinosaurs more generally, expanding the range of ecological adaptations recognized within this major clade.


Relative brain size
The Encephalization Quotient (EQ) provides a measure of the overall brain size of an organism relative to its mass 5,6 .The calculated reptile encephalization quotient 50 (REQ) range for T. neglectus indicates its brain was of average or below-average size for a reptile of its mass, smaller than those reported from all other neornithischians other than ceratopsids, and most similar to those of Triceratops and thyreophorans (Table 1).Even assuming a greater 60% 51 or 73% 25 endocranial fill, the REQ of T. neglectus still falls within the range of extant reptiles and below those observed in non-ceratopsid ceratopsians and ornithopods, as well as that estimated for Leaellynasaura (1.1-1.8 52 ), although the probable juvenile status of the latter specimen limits the paleoneurological conclusions that can be drawn from it 53 .To ensure comparability of results, REQs were re-calculated for other ornithischian taxa using updated brain tissue density, endocranial fill, and body mass estimates, where necessary (see "Methods").Re-calculated REQs of these taxa remain broadly similar to previous estimates, although with slight differences due to differences in the density of brain tissues and body masses used herein (Table 1).

Olfactory tract size and olfactory ratio
The olfactory tract of T. neglectus is large, with the olfactory bulbs making up ~ 3% of the total endocast volume (Supplementary Table S1), exceeding the relative volume exhibited by extant birds (including Apteryx) 54 and overlapping with values reported for rodents and lagomorphs 55 .The olfactory ratio provides a proxy for olfactory acuity in fossil taxa 56 .The calculated olfactory ratio of T. neglectus is also large, greater than observed in extant birds 57 and more comparable in magnitude to those of Euoplocephalus, Alligator, and predatory theropods than to Hypacrosaurus, Triceratops, or herbivorous theropods (Fig. 3a, Supplementary Table S2).However, the olfactory tract exhibits a high degree of allometric independence from the rest of the brain 58 making it difficult to generalise comparisons of absolute magnitudes across large phylogenetic scales.Phylogenetic generalised least squares (pgls) regressions of olfactory ratio against body mass were used to compare development of the olfactory tract among non-avian dinosaurs (see "Methods").A significant relationship was retrieved regardless of the topology used (Fig. 3a): further, comparison of residuals indicates that T. neglectus did indeed have a substantially larger olfactory ratio than expected for its size, more so than any other sampled taxon (Fig. 3b).

Hearing range
The calculated best hearing range 9 of T. neglectus occupies a narrow low-frequency range of ~ 1854 Hz (approx.296-2150 Hz), a frequency of best hearing 9,59 of ~ 1100-1200 Hz, and an upper limit of hearing 59 of 3051 Hz.This is robust to the choice of scaling relationship used, with best hearing frequency broadly similar whether derived from the length of the endosseous cochlear duct 9 or estimated basilar papilla length 59 (Supplementary Table S3).This hearing range is similar to those reported from some crocodilians (e.g., Caiman crocodylus, best hearing range = 300-2000 Hz, mean best hearing = 1150 Hz 60 ) and squamates (e.g., Chalcides occelatus, best hearing range = 300-2000 Hz, mean best hearing = 1150 Hz 61 ), but is lower than those of other small neornithischians (e.g.Dysalotosaurus, best hearing range = ~ 350-3850 Hz, mean best hearing = 2100 Hz 62 , see Discussion and Supplementary Table S3), and extant birds 9 .

Semicircular canals
Thescelosaurus exhibits a very long and slender anterior semicircular canal (ASC), relative to both the lateral (LSC) and posterior (PSC) semicircular canals.Comparison of semicircular canal height across Ornithischia reveals that T. neglectus has a tall ASC, low PSC, and large ASC height: PSC height ratio relative to its skull length (Fig. 4a-d), greater than that known from any other ornithischian (Fig. 4d).A significant relationship was resolved between PSC height and skull length but not ASC height and skull length (Fig. 4a, b).
Extant tetrapods generally orient the LSC horizontally when adopting a typical "alert" head posture ( 29 and references therein, but see 63 ).Orienting the LSC horizontally in T. neglectus (Fig. 2g) results in a slightly upturned head posture, with the tip of the premaxilla lying flush with the foramen magnum, and the oral margin inclined Table 1.Reptile encephalization quotient (REQ) values calculated for a range of ornithischian taxa.REQs were calculated for both 50% and 60% fills of the endocranial space by the brain.a Body mass estimate derived from stylopodial circumferences by 14 .b Body mass estimate derived from scale models by 163 .Other body masses were estimated from stylopodial circumferences by the authors listed in the source column.at ~ 6°.This differs from the ventrally deflected alert postures reconstructed for ankylosaurs 64 , ceratopsians 65,66 , Tenontosaurus 67 , hadrosaurs (Figs. 2, 3, 4 in 23 ) and many saurischians 29,68 , but similarly inclined postures have been reported for Dysalotosaurus 62 and the sauropodomorph Massospondylus 68 .

Sensory biology of Thescelosaurus neglectus
The reconstructed endocast of Thescelosaurus neglectus exhibits a combination of characters that are plesiomorphic for Ornithischia (elongate olfactory tract, expanded cerebral hemispheres 69 ), or at least widely distributed within the clade (short cochlear duct 62 , expansive dural peak 49,70 ) (see Supplementary Information).The endocast of T. neglectus differs from those of other ornithischians primarily in characters related to its sensory biology and ecology, exhibiting a unique combination of a limited hearing range, large olfactory ratio, low REQ, and elongate ASC (Fig. 5).
The short cochlear duct of T. neglectus suggests limited ability to discriminate low and high-frequency sounds relative to many other ornithischian taxa.Its calculated best hearing range (~ 296-2150 Hz) is narrower than (best-performing model p = 0.000164, R 2 = 0.846; median p = 0.000163, R 2 = 0.846).(c) anterior semicircular canal height against posterior semicircular canal height (best-performing model p = 0.012, R 2 = 0.481, median p = 0.0136, R 2 = 0.472).(d) anterior canal height divided by posterior canal height, against skull length (bestperforming model p = 0.00894, R 2 = 0.551; median p = 0.0222, R 2 = 0.458).Results are plotted by taxon and locomotor style (see Materials and methods for decisions on quadrupedal vs. bipedal taxa).Heights of the anterior and posterior semicircular canals measured as their maximum diameter measured perpendicular to the long axis of the lateral semicircular canal.All pgls regressions conducted across 100 phylogenetic trees: regression lines from the best performing of these iterations in red, the range across all trees given in grey.
that reported for the dryosaurid Dysalotosaurus (~ 350-3850 Hz 62 ), with Thescelosaurus exhibiting less sensitivity to higher frequencies, while also lacking the enhanced sensitivity toward low frequencies observed in lambeosaurines 23 .By contrast, the observed very high olfactory ratio, which correlates with olfactory acuity 56 , suggests an acute sense of smell in Thescelosaurus.Among ornithischians, comparably high olfactory ratios are also observed in ankylosaurs (Fig. 3a, b), for which manual surface-digging for buried food has been posited 71,72 .The robust forelimbs 33,73 and rostrally fused premaxillae 74 of Thescelosaurus could similarly have been used to unearth foodstuffs such as roots and tubers located via olfaction.

Relative brain size and encephalisation quotient
Relative brain size and the encephalization quotient have long been considered to correlate positively with increased cognitive ability and behavioural complexity [4][5][6]50 , and empirical studies have linked greater relative size of the brain with increased performance in cognitive tasks such as learning 75,76 , memory 77 , problem-solving 78 , behavioural flexibility 79 , and innovation 80,81 . Inreased absolute or relative brain size has also been widely linked to greater social cognition 80,[82][83][84] , as required in larger 85 (but see 86 ), more complex 82,83 , or competitive 86,87 groups, with the increased REQ and forebrain volume of styracosternan ornithopods likewise used to suggest large group sizes 25 and complex social interaction 23,88 .Consequently, the 'reptilian' REQ of T. neglectus may indicate a cognitive and behavioural range within that of extant reptiles, and less complex social interactions and/or smaller group sizes than in other sampled Late Cretaceous ornithischians.This would be consistent with the short cochlear duct, implying a lack of vocalizations and, in-turn, small aggregation sizes 9 , in Thescelosaurus, and also its lack of bony ornaments for use in intraspecific signalling and combat, as present in many other ornithischian taxa (see 18,19 , and references therein).Multiple small, probable juvenile, individuals of Thescelosaurus are preserved in a multi-taxon bonebed from the 'convenience store' locality of the Frenchman Formation 27 , providing possible counter-evidence for larger aggregations.However, it is presently unknown if this association Figure 5.Comparison of the endocast of T. neglectus with other ornithischians. Simplified phylogenyof Ornithischia, after 42 . Endocast (left) and endosseous labyrinths (right) are illustrated for (from top): the stegosaurid Stegosaurus (redrawn from 70 ), the ankylosaurid Euoplocephalus (redrawn from 70 ), the thescelosaurid Thescelosaurus, the dryosaurid Dysalotosaurus (redrawn from 49 ), the hadrosaurid Hypacrosaurus (redrawn from 23 ), the protoceratopsid Protoceratops (redrawn from 161 ), and the ceratopsid Pachyrhinosaurus (redrawn from 172 ).Endocast lengths are scaled in proportion to REQ 1/3 for each taxon (Table 1), with the REQ of Triceratops used to approximate that of Pachyrhinosaurus. Enosseous labyrinth heights are scaled in proportion to the ASC height: PSC height ratio of each taxon. Distribuion of sensorineural characters discussed in the text is indicated. Orn. = Ornithopoda. represens a genuine biological signal, or is instead the result of preservational biases 27 , and the total number of individuals is not reported.Among other thescelosaurids, multiple associations of 2-3 individuals, including adult-juvenile associations postulated to represent family groupings, are known from Oryctodromeus 22,89 and a new taxon from the Mussentuchit Member of the Cedar Mountain Formation 90 .This lends some tenuous support to similarly small group size in Thescelosaurus, although it is possible these proximate small Oryctodromeus groups belonged to a larger colony 89 .Ultimately, hypotheses of group sizes in Thescelosaurus are difficult to test.
Furthermore, any estimation of the neuroanatomy and behaviour of fossil animals is difficult, and comparison of brain size measurements alone, without reference to neural circuitry, is an oversimplification 91,92 .Moreover, most comparative cognitive studies have focused on mammals, which may be problematic given the fundamental differences between the pallia of extant mammals and birds 91 .Indeed, complex behaviours and advanced cognitive skills are known from extant reptiles despite their relatively low EQs 93 , and the validity of EQ as a measure of 'intelligence' is doubtful 91,94,95 , with work on primates suggesting absolute brain size is instead a better predictor of cognitive performance 94,95 .Despite its smaller overall endocast size, comparison of brain regions indicates that the cerebral hemispheres-responsible for 'higher' cognitive functions 85 -occupy ~ 30% of the total endocast volume in T. neglectus, a greater proportion than in some iguanodontians such as Dysalotosaurus (~ 16% 25 , see Supplementary Table S4).This may be a consequence of the relatively smaller brain size of Thescelosaurus; more complex patterns of cerebrum evolution in Neornithischia than previously recognized; or, alternatively, independent expansion of the cerebral hemispheres-and so, by inference, cognitive capacity-in the lineage leading to Thescelosaurus, parallel with the stepwise increases in forebrain volume observed within Iguanodontia [23][24][25]88,96 . Noneteless, the cerebral hemispheres of T. neglectus remain proportionately smaller than in Proa and most hadrosaurids (~ 40% [23][24][25] , see Supplementary Table S4).This, together with the absolutely smaller size of its endocast and lower REQ, suggests comparatively simple cognitive ability and less complex behaviours in T. neglectus than in coeval ornithopods, and the small absolute size of the endocast compared to ankylosaurids and neoceratopsians may also be notable.

Endocranial anatomy and agility in Thescelosaurus neglectus
Since its discovery, the locomotory performance of Thescelosaurus has been controversial.Although originally reconstructed as an agile, cursorial animal on the basis of its bipedal skeletal proportions and size 34 , subsequent authors have typically considered Thescelosaurus to have been poorly adapted to running due to its overall robust build and the structure of the hindlimb 33,35,36 .Specifically, adult Thescelosaurus exhibit a longer femur than tibia, and relatively short metatarsals 32,33,35,37 , unlike extant cursorial mammals, cursorial theropods, and the cursorial neornithischians Parksosaurus, Dryosaurus, Dysalotosaurus and Hypsilophodon 33,37 .Instead, it exhibits proportions more comparable to those observed in large hadrosaurids 33 , and it has been suggested that Thescelosaurus represented an independent acquisition of graviportality 33,36,37 , or possibly even facultative quadrupedality 33 , parallel to that observed in iguanodontian ornithopods.Despite this, Thescelosaurus does differ from graviportal iguanodontians in other hindlimb characters such as the more proximal location of the fourth trochanter of the femur 33,37 , resulting in a lower moment arm for the caudofemoralis musculature and faster, but less efficient, retraction of the hindlimb, an adaptation towards fast running also seen in taxa such as Parksosaurus, Hypsilophodon and Dryosaurus 33,37 .However, the fourth trochanter of Thescelosaurus is still situated more distally than in other thescelosaurids such as Koreanosaurus 97 , indicating reduced relative hindlimb retraction speed, but greater power, relative to immediate outgroups.Consequently, the bulk of the evidence suggests reduced cursoriality and greater hindlimb retraction power in Thescelosaurus relative to earlier-diverging thescelosaurids and outgroups.
The dimensions of the flocculus may provide indirect evidence of agility as a proxy for the size of the floccular lobes, which are important in gaze stabilization through coordinating the vestibular system with the muscles of the eyes and neck 98,99 .The small, indistinct flocculus observed here (Fig. 1f) implies reduced agility in Thescelosaurus, especially when compared to the large flocculi of Dryosaurus and Zephyrosaurus 48 .However, flocculus size decreases through ontogeny in Dysalotosaurus 49 , and small flocculi are also observed in taxa such as Hypsilophodon 48 which nonetheless shows clear postcranial correlates of cursoriality 37 .Moreover, the floccular fossa houses other structures in addition to the floccular lobe itself, and its size has been found to represent a poor proxy of locomotory mode in extant birds 99 , and likewise does not distinguish quadrupedal and bipedal ornithischians 100 .Consequently, the size of the flocculus appears an unreliable indicator of agility or locomotory behaviour in dinosaurs 99 , necessitating alternative proxies.
The small flocculus in T. neglectus contrasts with its extremely elongate anterior semicircular canal (Figs. 2, 4a,  d).The semicircular canals sense rotational acceleration of the head and help to coordinate gaze stabilization 7,98 , with elongation (increased radius) of the canals hypothesised to result in greater sensitivity 7,101 .Consequently, measurements of the semicircular canals may provide proxies for locomotory behaviour and agility in extinct organisms (e.g. 7,13,29,98,102, but see 12,103,104 ), and lengthening of the anterior semicircular canal (ASC), and probably also the posterior canal (PSC), which both sense balance (changes in pitch and roll), correlate with bipedality in dinosaurs 102 .Within ornithischians specifically, it has been suggested that the ratio between ASC height: PSC height positively correlates with locomotory agility 24 , based on the observation that the secondary evolution of quadrupedality and reduced agility in ornithopods is accompanied by a reduction in relative ASC height 24 .We find some support for this relationship here by recovering a significant relationship between PSC and skull length but not ASC and skull length, implying that PSC height is controlled by spatial constraints in the skull whereas ASC height varies with ecology.However, this is more likely a result of low statistical power due to the very small taxon sample size available here (n = 10-11), and these results should be considered provisional.Nonetheless, the extremely long ASC suggests acute balance sensitivity, and so possibly high agility, in Thescelosaurus.
In sum, synthesis of agility correlates across the skeleton of Thescelosaurus yield contradictory signals, with acute balance inferred from the ASC conflicting with the reduced cursoriality of the hindlimb.This conflict may www.nature.com/scientificreports/be due to ecological constraints on the hindlimb.Thescelosaurus inhabited coastal-plain environments including swamps and marshes 105 , and is more commonly found in channel and near-channel deposits 106,107 .Among large ungulates, semiaquatic taxa that have to travel through slippery or sticky muddy substrates exhibit less cursorial forelimbs, with greater leverage for the muscles powering propulsion 108 .Robust hindlimbs, adapted for stability and powerful retraction, may similarly have been more important for navigation of wet environments than typical cursorial adaptations in Thescelosaurus.Moreover, the short PSC (Fig. 4b) and unelongated LSC (Fig. 2)-responsible for sensing turning movements and important during navigation at high speeds 102-further suggests that T. neglectus was not highly agile but instead relatively graviportal, and that its acute balance sensitivity does not reflect locomotory performance.Instead, the expanded endosseous labyrinth of Thescelosaurus, in conjunction with other endocranial and skeletal data, leads us to alternative hypotheses.

Semi-fossorial behaviours in Thescelosaurus and other small neornithischians
Among vertebrates, the character combination preserved in T. neglectus is unique among sampled ornithischians (Fig. 3) but common to many fossorial and semi-fossorial taxa (although anatomical adaptations to fossoriality may differ markedly between clades 109 ).4][115][116] ); enhanced equilibrium sensitivity 117 of the ASC 8 , but not the LSC 118 or PSC 8 ; and more robust skeletal elements with less cursorial limbs 119,120 .
Although the phylogenetic position of Thescelosaurus remains controversial 38 , it is broadly considered to be phylogenetically proximate to Orodrominae within Neornithischia (e.g. 22,31,413][44][45][46] ).Compelling trace 22,89,121 and body fossil 22,73,122 evidence for fossorial behaviours are known from the orodromine Oryctodromeus, including individuals entombed within preserved subterranean burrows 22,89,121 .Morphological and sedimentological comparison suggests that other orodromine taxa (e.g., Orodromeus, Koreanosaurus, undescribed Mussentuchit thescelosaurid) were also burrowers 22,97,123,124 .Although Thescelosaurus lacks the same degree of anatomical specialization as seen in Oryctodromeus-such as the increased sacral count and pubosacral articulations, interpreted as adaptations towards reinforcing the pelvis against forces encountered when bracing the body using the hindlimbs and tail during digging 22,73,122-it does share several morphological characters that have been linked to burrowing in orodromines (Fig. 3b).These include partial fusion of the premaxillae 74 , which may have been used to loosen soil 22 ; robust forelimbs 33,73 ; and a broad scapula blade 33 with a strong ventral expansion 34,122 (note that, although this character is absent in "T." warreni 122,125 , this species has since been referred to Parksosaurus 31,126 ).This expansion of the scapula would have provided greater origination areas for muscle groups (deltoideus scapularis, teres major) important for force generation during manual scratch-digging 22,122 .
Regarding other ecological factors, the relatively large size of T. neglectus (up to ~ 4.1 m in total length 31 and 340 kg in mass 14 , relative to the 20 kg Orodromeus 14 ), may make burrowing appear unlikely.However, Oryctrodromeus individuals up to 3.5 m in length are known from burrow in-fills 89 , and fossilized tunnels have been attributed to substantially larger (up to 1200 kg) mammals 127 .Similarly, wet lowlands, the depositional environment of most Thescelosaurus specimens [105][106][107] , are interpreted by some authors as less suitable for burrowing 128 .However, sediments of the Mussentuchit Member of the Cedar Mountain Formation are notable for being deposited on a tidally influenced coastal plain with periodic saturation 129 , yet taphonomic evidence for burrowing exists in the form of dozens of skeletons of a new, as of yet unnamed species of thescelosaurid 123 .These specimens are interpreted as preserved in subterranean burrows due to their high relative overabundance and unusual levels of articulation compared to other elements of the fauna, and the presence of compacted (~ 1 m), near-complete, multi-individual specimens of multiple age classes 123,130 .Similar factors have been used to support evidence of burrowing in the thescelosaurids Koreanosaurus 97 and Orodromeus 124 in the absence of definitive burrow structures.Oryctodromeus is purportedly known from somewhat drier floodplain deposits 22 , although wet coastal deltaic deposits are noted for a large portion of the Blackleaf Formation 131,132 in which it occurs.Further, many extant animals-including crocodilians [133][134][135] and mammals 136,137-do burrow in wet environments, such as riverbanks and waterlogged low-lying areas.In short, periodically waterlogged soils, or riparian environments, do not preclude hypotheses of burrowing in thescelosaurids, and soil saturation may prove to be a limiting factor on burrow preservation, rather than on fossorial behaviour, in these dinosaurs.
Still, in the absence of any fossilized tunnels or other corroborating ichnological evidence (Fig. 6), the actual extent of fossorial behaviours by Thescelosaurus is unclear.The resolution of common 'fossorial' traits in Thescelosaurus (Fig. 6) indicates that semi-fossorial behaviours may, in fact, be plesiomorphic to Thescelosauridae, or more broadly distributed among Neornithischia in general.This also raises the possibility that the incomplete evidence of fossoriality in Thescelosaurus is a result of its divergence from semi-fossorial ancestors: indeed, the unusual character combination and parallelisms with iguanodontian ornithopods 33,36,37 observed in Thescelosaurus may ultimately be explicable through secondary reduction in fossoriality and concomitant increase in body size, although the taxonomic instability of Thescelosaurinae 38 makes this hypothesis difficult to evaluate.More comprehensive comparison of endocranial and skeletal anatomy across Neornithischia is necessary to further unravel these patterns of ecological evolution through the clade, including evaluation of characters potentially related to digging in other taxa.Nonetheless, taken together, sensorineural and gross morphological lines of evidence support the potential for burrowing behaviours in Thescelosaurus itself and/or evolutionary constraints in neurobiology resulting from specializations to a semi-fossorial lifestyle in pre-Maastrichtian thescelosaurids.
Regardless of the extent of fossorial behaviours in Thescelosaurus, the observation of endocranial features consistent with fossoriality from a dinosaur clade including known burrowers is significant.These results represent the first neurological specializations to fossoriality identified in any non-avian dinosaur, expanding the range of ecological adaptations recognized in this major clade.4][135] ) and Apteryx 138,139 , which each also exhibit high olfactory ratios 56,140 .Olfaction is also important in general surface foraging in these taxa [140][141][142] , and many birds excavate nesting tunnels (e.g. 143,144) without obvious morphological specializations, making the extent to which this character can be linked to burrowing in these taxa ambiguous.However, the early development and emphasis of an acute olfactory system may represent a specialization towards subterranean life in burrow-nesting hydrobatid chicks 145 , which navigate 146 and recognize individuals 146,147 via olfaction.
The identification of characters consistent with burrowing behaviours in Thescelosaurus, from the late Maastrichtian, is further interesting given that the extinction of non-avian dinosaurs across the K-Pg boundary has been attributed to an inability to find shelter 148 and collapse of primary productivity [149][150][151] following the bolide impact at the end of the Cretaceous.During this time, the ability both to shelter from climatic extremes underground and to locate and access hardy, yet buried, resources such as roots and rhizomes would have been critical 148 , and semi-fossorial habits have been suggested as important in the survival of mammalian taxa across this boundary 148,152,153 .The ability of at least some neornithischians to perform these behaviours 22 and, in Figure 6.Distribution of characters associated with fossoriality within Thescelosauridae.Simplified timescaled phylogeny of the Thescelosauridae, after 45,46 , with the positions of taxa of more labile placement in the clade indicated by dotted lines (cf. with 44 ).Taxon stratigraphic ranges (see "Methods") indicated by thick lines.Taxon silhouettes and known material from parts of the skeleton bearing discussed characters (skull, pectoral girdle, forelimb, pelvis, hindlimb) are illustrated.Distribution of the following characters and pieces of evidence consistent with fossorial habits (see 22,73,89,97,121,122 and main text) are indicated.Cranial (1-5): premaxillary fusion (1), reduced EQ (2), large olfactory bulbs (3), enlarged ASC (4), limited hearing range (5).Scapulacoracoid (6-9): fusion of scapula and coracoid (6), well-developed acromion (7), scapular spine (8), prominent posteroventral expansion of scapular blade (9).Pelvis and hindlimb (10-12): seven sacral vertebrae (10), pubosacral articulation (11), reduced cursoriality (12).Occurrence evidence (13-14): body fossils preserved in burrows (13), sedimentological evidence (14).Gross orodromine body shape broadly follows 89,173 , with specific reconstruction and illustrated skeletal anatomy of Changchunsaurus following 39 ; Oryctodromeus 22,89,122 ; Koreanosaurus 97 , with the holotype and paratype assumed to belong to a single individual after 97 ; Haya 45 ; Orodromeus 73,173 ; and Zephyrosaurus 47 , with postcranial elements reconstructed after those of Orodromeus 73,173 .Parksosaurus anatomy follows 45 .Thescelosaurus is reconstructed primarily from NCSM 15728 but with additional anatomical data and maximum estimated length from 31 .Character coding follows 22,39,[45][46][47][48]73,74,89,97,121,122 and discussion in the main text. Oro = Orodrominae. Scale bar for silhouettes = 1 m.

Conclusions
Virtual reconstruction of the endocast of Thescelosaurus neglectus reveals a slightly smaller endocast than expected for a reptile of its size and a restricted hearing range, combined with well-developed senses of olfaction and balance.These results contrast with patterns observed in contemporary ornithopods, suggesting that Thescelosaurus instead exhibited relatively small group sizes and cognitive abilities within the range of extant reptiles.This character combination, in conjunction with features of the appendicular skeleton, is consistent with burrowing behaviours, as inferred from trace and skeletal fossil evidence from related thescelosaurid taxa.These features may suggest similar semi-fossorial capability in T. neglectus or, alternatively, may have been inherited as evolutionary constraints from semi-fossorial ancestors.Indeed, the unusual character combination of Thescelosaurus could reflect a secondary reduction in fossoriality and concomitant increase in body size.Either way, these results suggest that semi-fossoriality may have been a general feature of the ecology of thescelosaurids, and potentially neornithischians more generally.Moreover, they provide the first potential neurological specializations to fossoriality identified in a non-avian dinosaur, expanding the range of ecological adaptations recognized within the clade.The identification of potential semi-fossorial capability in the latest Cretaceous Thescelosaurus expands our understanding of the ecological niches realized by non-avian dinosaurs and suggests nuance to hypothesized mechanisms explaining their extinction across the end-Cretaceous mass extinction.

Endocranial reconstruction
The skull of NCSM 15728 ('Willo'), an adult Thescelosaurus neglectus, was CT-scanned using a Nikon XTH 225 ST microCT scanner at Duke University, Durham, NC, at a resolution of 87.62 μm.Scan data were then imported into Avizo (version 9) for segmentation of separate braincase and skull roof elements.The skull of NCSM 15728 has suffered a mild degree of ventrolateral shearing (Fig. 1a), partially disarticulating the braincase (Fig. 1b, c).
In order to repair this damage, the braincase was retrodeformed following a stepwise procedure, as described in 30,154 .To achieve this, the individual elements of the braincase were first isolated, and minor cracks in them repaired, in the Avizo segmentation editor.Among the unpaired, midline elements of the braincase, the robust basisphenoid and basioccipital appear not to have suffered plastic deformation.By contrast, the distal tip of the dorsal process of the supraoccipital has been bent laterally; in order to restore symmetry to this element, the distal tip of the supraoccipital was segmented out individually and rotated back into place.The left posterolateral corner of the basioccipital of NCSM 15728 is not associated with the skull but instead in a block containing the postcrania: consequently, it was not scanned.Instead, the right and left halves of the basioccipital were segmented separately, with the right half then being mirrored to yield a symmetrical, composite basioccipital.It should be noted that the occipital condyle of this resulting composite element is still incomplete, but this has no influence on the reconstruction of endocranial tissues.
For each of the paired braincase elements, the better-preserved element was retained.The preservation of each element was judged on evidence of deformation (cracks, warping, asymmetry), topological constraints defined by surrounding elements of the braincase, and comparisons to the osteology of related taxa (e.g. 48).The left prootic and laterosphenoid are both well-preserved but have become disarticulated: these were moved back into articulation.Whereas the paraoccipital process of the right fused exoccipital and opisthotic is better preserved, the right margin of the foramen magnum has also been squashed medially.Consequently, the better-preserved ventral process of the left exoccipital-opisthotic was mirrored and positioned in place.Shearing of the skull roof has resulted in minor bending of the anterior ends of the frontals and slight deformation to part of their dorsal surface.The less warped left frontal was retained, and these slight deformations were repaired.Shearing has also resulted in crushing of the posterolateral wing of the right parietal: consequently, the left parietal was retained.These elements were then all mirrored to produce symmetrical paired elements.
These retrodeformed elements were all then rearticulated to produce a reconstruction of the undeformed braincase (Fig. 1d).Rearticulation was performed on the basis of the sutural surfaces of each element and topological constraints imposed by surrounding bones.Rearticulation began with the largest and most robust bones (the frontal, parietal, supraoccipital, exoccipital-opisthotic, basioccipital and basisphenoid), helping to constrain the positions of the smaller, and potentially more susceptible to taphonomic deformation and translation, prootics and laterosphenoids.The reconstructed braincase was then tested against three further criteria: its bilateral symmetry, overall dimensional constraints imposed by the rest of the skull, and the continuous alignment of the semi-circular canals within the prootic and supraoccipital.These multiple lines of testing, and the stepwise procedure used herein 154 , are intended to maximise rigour, and minimise biases, in the reconstruction of the original dimensions of the braincase.
The endocranial spaces of the restored braincase were then isolated using the segmentation editor in Avizo.This resulted in endocasts of the dural envelope (and, by extension, the brain within) and the semi-circular canals and cochlear duct of the inner ear (Fig. 1e).In addition, the major nerves and blood vessels that drain the brain were reconstructed on the basis of foramina and other osteological correlates on the braincase (e.g. 29,69).The orbitosphenoids were not ossified in Thescelosaurus, as typical for thescelosaurids and early-diverging ornithopods 74 .However, their original ventral extent is inferred to lie at the position of a boss on the anterolateral surface of the laterosphenoids 74 , as observed in some ornithopods 48 .As orbitosphenoids are unknown from phylogenetically proximate taxa, no attempt was made to reconstruct them here.Instead, the position of this boss was used to Vol:.( 1234567890

Endocranial size and reptile encephalization quotient
The total volume of these endocranial reconstructions was measured in Avizo, using the 'Surface Area Volume' module.The resulting maximum and minimum endocranial volumes of Thescelosaurus, excluding the olfactory tract, were used to calculate the Encephalization Quotient 5,6 (EQ), which compares observed brain volume with that expected from body mass.The non-avian Reptile Encephalization Quotient (REQ) was calculated using the equation of 50 , as follows: where M Br = mass of the brain in grams, and M bd = body mass, in grams.M Br is calculated by multiplying the measured volume by a density of 1.036gcm −3 for brain tissues 98 .The brain of Thescelosaurus was estimated to fill 50% of the endocranial volume, as typical for studies on non-avian dinosaurs 4,6 .Preserved valleculae on the endocranial surfaces of some cerapodan ornithischians 51 have been used to suggest that the brain filled a larger proportion of the endocranial volume, up to ~ 60% 23,51,88,96 or even 73% or higher 25 .Although these valleculae were not observed in NCSM 15728 they are known from Thescelosaurus assiniboiensis 27 : consequently, a range of REQ values was calculated using fill estimates of both 50% and 60%.Body mass in extinct bipeds can be calculated from the circumference of the femur, employing scaling equations derived from extant taxa 155 .Herein, the mass estimate for a skeletally mature Thescelosaurus neglectus of 14 was employed.This mass estimate was derived from AMNH 5891, a specimen of equal femur length, and similar overall dimensions, to NCSM 15728, and so is expected to provide a reasonable estimate of the mass of this individual.
To place these results in a broader phylogenetic context, they were synthesized with previous measures of REQ from ornithischians.In order to compare these results with those of T. neglectus, brain masses were recalculated from reported endocranial volumes (excluding the olfactory tract 4,5 ) assuming a density of 1.036gcm −3 for brain tissues 98 .For the sake of comparison, REQs were calculated for estimates of the brain as occupying both 50% and 60% of the endocranial space, although a 60% fill is only likely for some neornithischians (see above).Multiple methods exist to estimate the body mass of extinct taxa, varying from scaling equations through to volumetric models, and different methods may retrieve very different results 156,157 .Previous estimates of ornithischian REQs have employed a combination of these methods, introducing systematic biases into comparisons between them.In an attempt to standardize comparisons between T. neglectus and other taxa, previously reported REQs were re-calculated using updated body mass estimates as derived from scaling equations of stylopodial circumferences 14,155,157 wherever possible.REQs were re-calculated for a specimen of Psittacosaurus lujiatunensis (PKUP V1060) using data presented by 158 , but assuming a 50-60% fill of the endocranial spaces by the brain tissues.Similarly, the REQ of Proa valdearinnoensis was re-calculated from data from 25 , but using endocranial fill estimates of 50-60%.REQs for specimens of Iguanodon bernissartensis (RBINS R51), Lurdusaurus arenatus (MNHN GDF 1700) and Mantellisaurus atherfieldensis (RBINS R57) were re-calculated using the endocranial volumes reported by 96 and the body mass estimates calculated for these same specimens by 14 .Iguanodon and Lurdusaurus were considered quadrupedal after 17,159 , and Mantellisaurus as at least facultatively bipedal after 17 , and so the quadrupedal and bipedal mass estimates 14 were used for these taxa, respectively.Hadrosaurids are considered to have been primarily quadrupedal (e.g. 17 ): consequently, only the larger, quadrupedal, mass estimate for Amurosaurus riabinini of 88 was used herein.The REQ of Kentrosaurus aethiopicus 6,50 was also updated using the body mass estimate for a composite skeleton of this taxon calculated by 14 .
The REQ of Euoplocephalus was derived from the endocranial volume of AMNH 5337, as calculated by 6 , and the body mass of the similarly-sized and proportioned 160 AMNH 5404, as calculated by 14 .Similarly, the REQ of Protoceratops andrewsi was derived from the endocranial volume of AMNH 6466, a large adult 161 , as calculated by 4 , and the body mass estimate of AMNH 6424, a similarly-sized large adult, of 14 .The endocranial data from Hypacrosaurus altispinus used herein comes the reconstruction of ROM 702 by 23 .The body mass of ROM 702 was approximated from the similarly-sized but more complete specimen CMN 8501, following 23 , using the quadrupedal mass estimate of 14 .
The endocranial volume of Camptosaurus dispar was calculated by 4 from YPM VP 1880, a medium-sized individual, approximately two-thirds the length of a large Camptosaurus 162 .Consequently, the 400 kg body mass estimate used by 4 for this specimen, as derived from the scale models of 163 , was retained here as it appears plausible when compared with the 1000-1300 kg estimate calculated from the stylopodial circumferences of a large adult Camptosaurus by 14 .The endocranial volumes of Stegosaurus, Edmontosaurus and Triceratops of 4,50 were derived from specimens lacking sufficient postcranial material from which to derive estimates of body mass.Consequently, to accommodate the range of uncertainty in these taxa, maximum and minimum REQs were calculated from minimum and maximum estimates of body mass, respectively.The minimum body mass estimates were taken from the scale models of 163 , as used in previous estimations of REQ in these taxa 4,50 , whereas the body masses of large individuals of Stegosaurus ungulatus, Edmontosaurus annectens and Triceratops horridus, as calculated from stylopodial circumferences by 14 , were used as maximum body mass estimates.It should be noted that volumetric methods typically retrieve lower body mass estimates for very large taxa than do scaling equations 156,157 : consequently, the maximum REQ estimates for these taxa are almost certainly too large compared to other sampled ornithischians.Nevertheless, as two of these taxa (Stegosaurus and Triceratops) exhibit two of the lowest REQ values in the sample, the maximum REQ values will represent a conservative estimate of their brain size relative to other taxa.

Endosseous labyrinth and hearing range
The length of the endosseous cochlear duct was also measured in the Avizo viewer.This was then scaled against basicranial length (taken as the length of the basioccipital and basisphenoid, not including the parasphenoid rostrum) and used to calculate the Best Frequency Range (BFR) and Mean Best Hearing (MBH) using the equations of 9 , as follows: where ECD = Log 10 (scaled endosseous cochlear duct length).
For comparison, the Best Frequency of hearing (BF) and Maximum Frequency (MF) of hearing were also calculated using the equations of 59 , as follows: where L = the length of the basilar papilla, in mm.As the length of the basilar papilla is unknown in Thescelosaurus, it was estimated as being equal to 2/3rds the length of the endosseous cochlear duct, following 59 .Measurements of the maximum vertical diameter (height) and horizontal diameter (width) of the anterior semicircular canal (ASC) and posterior semicircular canal (PSC), with the labyrinth oriented so the lateral semicircular canal (LSC) lay horizontally, were taken in the Avizo viewer.Further, the total length of each of the semicircular canals was also measured as the length of a line drawn through the centre of the lumen of each in three dimensions.

Phylogenetic tree for comparative paleoneurology
To interpret data from T. neglectus in a broader context, an updated version of the informal dinosaurian supertree of 164 was produced, resulting in a time-scaled species-level topology of 447 taxa (see Supplementary Information for details on tree construction, and Supplementary Data SD1 and SD2 for dated trees).Due to the uncertain phylogenetic position of Thescelosaurus two alternative backbone topologies were used for Cerapoda.The first includes Thescelosaurus and related taxa as early-diverging ornithopods (e.g. 40,41), with branching order within Ornithopoda following 41 .The second instead treats Thescelosaurus, other thescelosaurines, and orodromines in a monophyletic, non-cerapodan, Thescelosauridae, following [42][43][44] .

Olfactory ratio in Thescelosaurus neglectus and comparison with other archosaurs
The olfactory ratio 56 of T. neglectus was calculated as the ratio of the longest diameter of the olfactory bulb: longest diameter of the cerebral hemispheres, as measured from the endocast in dorsal view in the Avizo viewer.This measurement was taken in two ways, as illustrated in 56 : directly measured from the reconstructed endocast, and also from the maximum width of the fossae for the olfactory bulbs and cerebrum in the skull roof.Both of these methods retrieved identical results.To compare this result to other archosaurs, the olfactory ratio of T. neglectus was Log 10 transformed and combined with the theropod-focused dataset of 56 (although omitting "Troodon formosus" due to the invalidity of that taxon 165 , and taxonomic instability of formerly referred material 166 ) and ornithischian-focused dataset of 66 , with additional data on Erlikosaurus from 167 .CMN 34825, a subadult 23 Corythosaurus sp., was excluded from this analysis due to its ontogenetic status.In order to estimate a regression line for Dinosauria, Alligator data were excluded.Phylogenetic generalized least-squares (pgls) regressions 168 were then performed between olfactory ratio and body mass as a predictor variable for the remaining sample of dinosaur taxa (n = 25), using the pgls function within the 'caper' R 169 package 170 , with maximum likelihood estimation of Pagel's lambda 171 , the phylogenetic signal parameter.Model performance was compared using log likelihoods and the small-sample corrected Aikaike Information Criterion (AICc).The residuals from this regression were then plotted to compare Thescelosaurus with other dinosaur taxa.The data used in these analyses is provided in Supplementary Data item SD3, and the full results in SD4.

Relative vertical semicircular canal development in Thescelosaurus and other ornithischians
The relative height of the ASC and PSC has been suggested to correlate with locomotory agility in ornithischians 24 .To compare the height of the vertical semicircular canals across ornithischian taxa, the vertical height (= maximum vertical diameter with the LSC oriented horizontally, see above) of the ASC and PSC of T. neglectus were combined with the dataset of 66 and measurements collected from published digital reconstructions of ornithischian taxa.Pgls regressions were then performed between each of anterior semicircular canal height, posterior canal height, and the ratio between the two as dependent variables, and basal skull length as a predictor variable.All data was Log 10 -transformed prior to analysis.Skull length was preferred for comparison to semicircular canal measurements as head size will be more relevant to their development than total body mass 102 .No attempt was made to calculate head mass due to the lack of data for this attribute in non-avian dinosaurs.The data used in these analyses is provided in Supplementary Data item SD5, and the full results SD6.
, resolution of acute olfaction, ability to unearth buried foodstuffs, and possible burrowing capability in the latest Cretaceous Thescelosaurus, suggest that such survivorship scenarios may be oversimplified, and more nuanced explanations are necessary to explain the extinction of small-bodied non-avian dinosaurs at the end of the Cretaceous.